Rediscovering ACE: Novel insights into the many roles of the angiotensin-converting enzyme

Journal of Molecular Medicine

Volumn 91, Issue 10, 2013, Pages 1143-1154

  Gonzalez Villalobos, Romer A ^a   Shen, Xiao Z ^a   Bernstein, Ellen A ^a   Janjulia, Tea ^a   Taylor, Brian ^a   Giani, Jorge F ^a   Blackwell, Wendell Lamar B ^a   Shah, Kandarp H ^a   Shi, Peng D ^a   Fuchs, Sebastien ^a   Bernstein, Kenneth E ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Ac SDKP; Angiotensin II; Antigen processing; Blood pressure; Kidney function; MHC class I

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; ANGIOTENSINOGEN; DIPEPTIDYL CARBOXYPEPTIDASE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; RENIN; TUMOR NECROSIS FACTOR ALPHA;

ALLELE; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANGIOTENSIN BLOOD LEVEL; CARBOXY TERMINAL SEQUENCE; CD8+ T LYMPHOCYTE; ELEVATED BLOOD PRESSURE; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GENE DELETION; GENE INSERTION; GENETIC POLYMORPHISM; GENOTYPE; GLOMERULUS FILTRATION RATE; HEART FAILURE; HEART INFARCTION; HOMOLOGOUS RECOMBINATION; HUMAN; HYDRONEPHROSIS; HYPERTENSION; HYPOTENSION; IMMUNITY; INFLAMMATION; KIDNEY CONCENTRATING CAPACITY; KIDNEY MEDULLA; KIDNEY PLASMA FLOW; KIDNEY PROXIMAL TUBULE; MESANGIUM CELL; NONHUMAN; PHENOTYPE; POINT MUTATION; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SYSTOLIC BLOOD PRESSURE; THERMOSTABILITY; TISSUE DISTRIBUTION; URINE; VASCULAR ENDOTHELIUM;

ANIMALS; CYTOKINES; ENDOTHELIAL CELLS; GENE EXPRESSION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; HYPERTENSION; IMMUNITY; IMMUNOLOGIC MEMORY; KIDNEY; MICE; MICE, KNOCKOUT; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; PHENOTYPE; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84885321616     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1051-z     Document Type: Review

References (101)

1. Skeggs LT Jr, Kahn JR, Shumway NP (1956) The preparation and function of the hypertensin-converting enzyme. J Exp Med 103:295-299
2. Erdos EG, Skidgel RA (1987) The angiotensin I-converting enzyme. Lab Invest 56:345-348
3. Skidgel RA, Engelbrecht S, Johnson AR, Erdos EG (1984) Hydrolysis of substance p and neurotensin by converting enzyme and neutral endopeptidase. Peptides 5:769-776
4. Skidgel RA, Erdos EG (1985) Novel activity of human angiotensin I converting enzyme: release of the NH2- and COOH-terminal tripeptides from the luteinizing hormone-releasing hormone. Proc Natl Acad Sci U S A 82:1025-1029
5. Azizi M, Ezan E, Nicolet L, Grognet J-M, Menard J (1997) High plasma level of N-acetyl-seryl-aspartyl-lysyl-proline: a new marker of chronic angiotensin-converting enzyme inhibition. Hypertension 30:1015-1019
6. Soubrier F, Alhenc-Gelas F, Hubert C, Allegrini J, John M, Tregear G, Corvol P (1988) Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc Natl Acad Sci U S A 85:9386-9390
7. Bernstein KE, Martin BM, Edwards AS, Bernstein EA (1989) Mouse angiotensin-converting enzyme is a protein composed of two homologous domains. J Biol Chem 264:11945-11951
8. Bernstein KE, Ong FS, Blackwell WL, Shah KH, Giani JF, Gonzalez-Villalobos RA, Shen XZ, Fuchs S, Touyz RM (2013) A modern understanding of the traditional and nontraditional biological functions of angiotensin-converting enzyme. Pharmacol Rev 65:1-46. doi: 10.1124/pr.112.006809
9. Ng KK, Vane JR (1967) Conversion of angiotensin I to angiotensin II. Nature 216:762-766
10. Alhenc-Gelas F, Baussant T, Hubert C, Soubrier F, Corvol P (1989) The angiotensin converting enzyme in the kidney. J Hypertens Suppl 7:S9-S13 (discussion S14)
11. Dorin JR (1995) Development of mouse models for cystic fibrosis. J Inherit Metab Dis 18:495-500
12. Chegary M, Brinke H, Ruiter JP, Wijburg FA, Stoll MS, Minkler PE, van Weeghel M, Schulz H, Hoppel CL, Wanders RJ et al (2009) Mitochondrial long chain fatty acid beta-oxidation in man and mouse. Biochim Biophys Acta 1791:806-815. doi: 10.1016/j.bbalip.2009.05.006
13. King-Underwood L, Little S, Baker M, Clutterbuck R, Delassus S, Enver T, Lebozer C, Min T, Moore A, Schedl A et al (2005) Wt1 is not essential for hematopoiesis in the mouse. Leuk Res 29:803-812. doi: 10.1016/j.leukres.2004.11. 020
14. Kobayashi Y (2010) The regulatory role of nitric oxide in proinflammatory cytokine expression during the induction and resolution of inflammation. J Leukoc Biol 88:1157-1162. doi: 10.1189/jlb.0310149
15. Keller C, Capecchi MR (2005) New genetic tactics to model alveolar rhabdomyosarcoma in the mouse. Cancer Res 65:7530-7532. doi: 10.1158/0008-5472.CAN-05-0477
16. Makki N, Capecchi MR (2012) Cardiovascular defects in a mouse model of HOXA1 syndrome. Hum Mol Genet 21:26-31. doi: 10.1093/hmg/ddr434
17. Krege JH, John SW, Langenbach LL, Hodgin JB, Hagaman JR, Bachman ES, Jennette JC, O'Brien DA, Smithies O (1995) Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375:146-148. doi: 10.1038/375146a0
18. Esther CR Jr, Howard TE, Marino EM, Goddard JM, Capecchi MR, Bernstein KE (1996) Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab Invest 74:953-965
19. Kim HS, Krege JH, Kluckman KD, Hagaman JR, Hodgin JB, Best CF, Jennette JC, Coffman TM, Maeda N, Smithies O (1995) Genetic control of blood pressure and the angiotensinogen locus. Proc Natl Acad Sci U S A 92:2735-2739
20. Tanimoto K, Sugiyama F, Goto Y, Ishida J, Takimoto E, Yagami K, Fukamizu A, Murakami K (1994) Angiotensinogen-deficient mice with hypotension. J Biol Chem 269:31334-31337
21. Niimura F, Labosky PA, Kakuchi J, Okubo S, Yoshida H, Oikawa T, Ichiki T, Naftilan AJ, Fogo A, Inagami T et al (1995) Gene targeting in mice reveals a requirement for angiotensin in the development and maintenance of kidney morphology and growth factor regulation. J Clin Invest 96:2947-2954. doi: 10.1172/JCI118366
22. Tsuchida S, Matsusaka T, Chen X, Okubo S, Niimura F, Nishimura H, Fogo A, Utsunomiya H, Inagami T, Ichikawa I (1998) Murine double nullizygotes of the angiotensin type 1A and 1B receptor genes duplicate severe abnormal phenotypes of angiotensinogen nullizygotes. J Clin Invest 101:755-760. doi: 10.1172/JCI1899
23. Takahashi N, Lopez ML, Cowhig JE Jr, Taylor MA, Hatada T, Riggs E, Lee G, Gomez RA, Kim HS, Smithies O (2005) Ren1c homozygous null mice are hypotensive and polyuric, but heterozygotes are indistinguishable from wild-type. J Am Soc Nephrol 16:125-132
24. Manolis A, Doumas M (2008) Sexual dysfunction: the 'prima ballerina' of hypertension-related quality-of-life complications. J Hypertens 26:2074-2084. doi: 10.1097/HJH.0b013e32830dd0c6
25. Lin C, Datta V, Okwan-Duodu D, Chen X, Fuchs S, Alsabeh R, Billet S, Bernstein KE, Shen XZ (2011) Angiotensin-converting enzyme is required for normal myelopoiesis. FASEB J 25:1145-1155. doi: 10.1096/fj.10-169433
26. Pratt MC, Lewis-Barned NJ, Walker RJ, Bailey RR, Shand BI, Livesey J (1992) Effect of angiotensin converting enzyme inhibitors on erythropoietin concentrations in healthy volunteers. Br J Clin Pharmacol 34:363-365
27. Friberg P, Sundelin B, Bohman SO, Bobik A, Nilsson H, Wickman A, Gustafsson H, Petersen J, Adams MA (1994) Renin-angiotensin system in neonatal rats: induction of a renal abnormality in response to ACE inhibition or angiotensin II antagonism. Kidney Int 45:485-492
28. Guron G, Adams MA, Sundelin B, Friberg P (1997) Neonatal angiotensin-converting enzyme inhibition in the rat induces persistent abnormalities in renal function and histology. Hypertension 29:91-97
29. Pryde PG, Sedman AB, Nugent CE, Barr M Jr (1993) Angiotensin-converting enzyme inhibitor fetopathy. J Am Soc Nephrol 3:1575-1582
30. Quan A (2006) Fetopathy associated with exposure to angiotensin converting enzyme inhibitors and angiotensin receptor antagonists. Early Hum Dev 82:23-28. doi: 10.1016/j.earlhumdev.2005.11.001
31. Cole J, Quach DL, Sundaram K, Corvol P, Capecchi MR, Bernstein KE (2002) Mice lacking endothelial angiotensin-converting enzyme have a normal blood pressure. Circ Res 90:87-92
32. Hooper NM, Turner AJ (1987) Isolation of two differentially glycosylated forms of peptidyl-dipeptidase A (angiotensin converting enzyme) from pig brain: a re-evaluation of their role in neuropeptide metabolism. Biochem J 241:625-633
33. Xiao HD, Fuchs S, Campbell DJ, Lewis W, Dudley SC Jr, Kasi VS, Hoit BD, Keshelava G, Zhao H, Capecchi MR et al (2004) Mice with cardiac-restricted angiotensin-converting enzyme (ACE) have atrial enlargement, cardiac arrhythmia, and sudden death. Am J Pathol 165:1019-1032. doi: 10.1016/S0002-9440(10)63363-9
34. Shen XZ, Li P, Weiss D, Fuchs S, Xiao HD, Adams JA, Williams IR, Capecchi MR, Taylor WR, Bernstein KE (2007) Mice with enhanced macrophage angiotensin-converting enzyme are resistant to melanoma. Am J Pathol 170:2122-2134
35. Smithies O, Kim HS, Takahashi N, Edgell MH (2000) Importance of quantitative genetic variations in the etiology of hypertension. Kidney Int 58:2265-2280. doi: 10.1046/j.1523-1755.2000.00411.x
36. Beneteau-Burnat B, Baudin B, Morgant G, Baumann FC, Giboudeau J (1990) Serum angiotensin-converting enzyme in healthy and sarcoidotic children: comparison with the reference interval for adults. Clin Chem 36:344-346
37. Tiret L, Rigat B, Visvikis S, Breda C, Corvol P, Cambien F, Soubrier F (1992) Evidence, from combined segregation and linkage analysis, that a variant of the angiotensin I-converting enzyme (ACE) gene controls plasma ACE levels. Am J Hum Genet 51:197-205
38. Rigat B, Hubert C, Alhenc-Gelas F, Cambien F, Corvol P, Soubrier F (1990) An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J Clin Invest 86:1343-1346. doi: 10.1172/JCI114844
39. Zhu X, Bouzekri N, Southam L, Cooper RS, Adeyemo A, McKenzie CA, Luke A, Chen G, Elston RC, Ward R (2001) Linkage and association analysis of angiotensin I-converting enzyme (ACE)-gene polymorphisms with ACE concentration and blood pressure. Am J Hum Genet 68:1139-1148. doi: 10.1086/320104
40. Levy D, DeStefano AL, Larson MG, O'Donnell CJ, Lifton RP, Gavras H, Cupples LA, Myers RH (2000) Evidence for a gene influencing blood pressure on chromosome 17. Genome scan linkage results for longitudinal blood pressure phenotypes in subjects from the Framingham heart study. Hypertension 36:477-483
41. Cambien F, Poirier O, Lecerf L, Evans A, Cambou JP, Arveiler D, Luc G, Bard JM, Bara L, Ricard S et al (1992) Deletion polymorphism in the gene for angiotensin-converting enzyme is a potent risk factor for myocardial infarction. Nature 359:641-644. doi: 10.1038/359641a0
42. Agerholm-Larsen B, Nordestgaard BG, Tybjaerg-Hansen A (2000) ACE gene polymorphism in cardiovascular disease: meta-analyses of small and large studies in whites. Arterioscler Thromb Vasc Biol 20:484-492
43. Cushman DW, Cheung HS (1971) Concentrations of angiotensin-converting enzyme in tissues of the rat. Biochim Biophys Acta 250:261-265
44. Soffer RL (1981) Angiotensin-converting enzyme. Wiley, New York
45. Esther CR, Marino EM, Howard TE, Machaud A, Corvol P, Capecchi MR, Bernstein KE (1997) The critical role of tissue angiotensin-converting enzyme as revealed by gene targeting in mice. J Clin Invest 99:2375-2385. doi: 10.1172/jci119419
46. Das M, Hartley JL, Soffers RL (1977) Serum angiotensin-converting enzyme. Isolation and relationship to the pulmonary enzyme. J Biol Chem 252:1316-1319
47. Woodman ZL, Oppong SY, Cook S, Hooper NM, Schwager SL, Brandt WF, Ehlers MR, Sturrock ED (2000) Shedding of somatic angiotensin-converting enzyme (ACE) is inefficient compared with testis ACE despite cleavage at identical stalk sites. Biochem J 347(Pt 3):711-718
48. Guyton AC (1991) Blood pressure control - special role of the kidneys and body fluids. Science 252:1813-1816
49. Coffman TM (2011) Under pressure: the search for the essential mechanisms of hypertension. Nat Med 17:1402-1409. doi: 10.1038/nm.2541
50. Komlosi P, Fuson AL, Fintha A, Peti-Peterdi J, Rosivall L, Warnock DG, Bell PD (2003) Angiotensin I conversion to angiotensin II stimulates cortical collecting duct sodium transport. Hypertension 42:195-199. doi: 10.1161/01.HYP.0000081221.36703.01
51. Casarini DE, Boim MA, Stella RC, Krieger-Azzolini MH, Krieger JE, Schor N (1997) Angiotensin I-converting enzyme activity in tubular fluid along the rat nephron. Am J Physiol 272:F405-F409
52. Gonzalez-Villalobos RA, Billet S, Kim C, Satou R, Fuchs S, Bernstein KE, Navar LG (2011) Intrarenal angiotensin-converting enzyme induces hypertension in response to angiotensin I infusion. J Am Soc Nephrol 22:449-459. doi: 10.1681/ASN.2010060624
53. Gonzalez-Villalobos RA, Satou R, Ohashi N, Semprun-Prieto LC, Katsurada A, Kim C, Upchurch GM, Prieto MC, Kobori H, Navar LG (2010) Intrarenal mouse renin-angiotensin system during ANG II-induced hypertension and ACE inhibition. Am J Physiol Renal Physiol 298:F150-F157. doi: 10.1152/ajprenal.00477.2009
54. Navar LG, Kobori H, Prieto MC, Gonzalez-Villalobos RA (2011) Intratubular renin-angiotensin system in hypertension. Hypertension 57:355-362. doi: 10.1161/HYPERTENSIONAHA.110.163519
55. Yosipiv IV, Dipp S, El-Dahr SS (1994) Ontogeny of somatic angiotensin-converting enzyme. Hypertension 23:369-374
56. Traynor T, Yang T, Huang YG, Krege JH, Briggs JP, Smithies O, Schnermann J (1999) Tubuloglomerular feedback in ACE-deficient mice. Am J Physiol 276:F751-F757
57. Hashimoto S, Adams JW, Bernstein KE, Schnermann J (2005) Micropuncture determination of nephron function in mice without tissue angiotensin-converting enzyme. Am J Physiol Renal Physiol 288:F445-F452. doi: 10.1152/ajprenal.00297. 2004
58. Atlas SA (2007) The renin-angiotensin aldosterone system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm 13:9-20
59. Lavoie JL, Lake-Bruse KD, Sigmund CD (2004) Increased blood pressure in transgenic mice expressing both human renin and angiotensinogen in the renal proximal tubule. Am J Physiol Renal Physiol 286:F965-F971
60. Sachetelli S, Liu Q, Zhang SL, Liu F, Hsieh TJ, Brezniceanu ML, Guo DF, Filep JG, Ingelfinger JR, Sigmund CD et al (2006) RAS blockade decreases blood pressure and proteinuria in transgenic mice overexpressing rat angiotensinogen gene in the kidney. Kidney Int 69:1016-1023
61. Kobori H, Ozawa Y, Satou R, Katsurada A, Miyata K, Ohashi N, Hase N, Suzaki Y, Sigmund CD, Navar LG (2007) Kidney-specific enhancement of ANG II stimulates endogenous intrarenal angiotensinogen in gene-targeted mice. Am J Physiol Renal Physiol 293:F938-F945. doi: 10.1152/ajprenal.00146.2007
62. Ying J, Stuart D, Hillas E, Gociman BR, Ramkumar N, Lalouel JM, Kohan DE (2012) Overexpression of mouse angiotensinogen in renal proximal tubule causes salt-sensitive hypertension in mice. Am J Hypertens 25:684-689. doi: 10.1038/ajh.2012.16
63. Imig JD, Navar GL, Zou LX, O'Reilly KC, Allen PL, Kaysen JH, Hammond TG, Navar LG (1999) Renal endosomes contain angiotensin peptides, converting enzyme, and AT(1A) receptors. Am J Physiol 277:F303-F311
64. Ingert C, Grima M, Coquard C, Barthelmebs M, Imbs JL (2002) Contribution of angiotensin II internalization to intrarenal angiotensin II levels in rats. Am J Physiol Renal Physiol 283:F1003-F1010
65. Vio CP, Jeanneret VA (2003) Local induction of angiotensin-converting enzyme in the kidney as a mechanism of progressive renal diseases. Kidney Int Suppl: S57-S63
66. Gonzalez-Villalobos RA, Janjulia T, Fletcher NK, Giani JF, Nguyen MT, Riquier-Brison AD, Seth D, Fuchs S, Eldari D, Picard N et al (2013) The absence of intrarenal ACE protects against hypertension. J Clin Invest 123:2011-2023
67. Ehlers MR, Riordan JF (1991) Angiotensin-converting enzyme: zinc- and inhibitor-binding stoichiometries of the somatic and testis isozymes. Biochemistry 30:7118-7126
68. Wei L, Alhenc-Gelas F, Corvol P, Clauser E (1991) The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J Biol Chem 266:9002-9008
69. Binevski PV, Sizova EA, Pozdnev VF, Kost OA (2003) Evidence for the negative cooperativity of the two active sites within bovine somatic angiotensin-converting enzyme. FEBS Lett 550:84-88
70. Woodman ZL, Schwager SL, Redelinghuys P, Carmona AK, Ehlers MR, Sturrock ED (2005) The N domain of somatic angiotensin-converting enzyme negatively regulates ectodomain shedding and catalytic activity. Biochem J 389:739-744. doi: 10.1042/BJ20050187
71. Fuchs S, Xiao HD, Cole JM, Adams JW, Frenzel K, Michaud A, Zhao H, Keshelava G, Capecchi MR, Corvol P et al (2004) Role of the N-terminal catalytic domain of angiotensin-converting enzyme investigated by targeted inactivation in mice. J Biol Chem 279:15946-15953. doi: 10.1074/jbc.M400149200
72. Fuchs S, Xiao HD, Hubert C, Michaud A, Campbell DJ, Adams JW, Capecchi MR, Corvol P, Bernstein KE (2008) Angiotensin-converting enzyme C-terminal catalytic domain is the main site of angiotensin I cleavage in vivo. Hypertension 51:267-274. doi: 10.1161/hypertensionaha.107.097865
73. Rousseau A, Michaud A, Chauvet MT, Lenfant M, Corvol P (1995) The hemoregulatory peptide N-acetyl-Ser-Asp-Lys-Pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J Biol Chem 270:3656-3661
74. Lenfant M, Wdzieczak-Bakala J, Guittet E, Prome JC, Sotty D, Frindel E (1989) Inhibitor of hematopoietic pluripotent stem cell proliferation: purification and determination of its structure. Proc Natl Acad Sci U S A 86:779-782
75. Liao TD, Yang XP, D'Ambrosio M, Zhang Y, Rhaleb NE, Carretero OA (2010) N-Acetyl-seryl-aspartyl-lysyl-proline attenuates renal injury and dysfunction in hypertensive rats with reduced renal mass: council for high blood pressure research. Hypertension 55:459-467. doi: 10.1161/HYPERTENSIONAHA.109.144568
76. Lin CX, Rhaleb NE, Yang XP, Liao TD, D'Ambrosio MA, Carretero OA (2008) Prevention of aortic fibrosis by N-acetyl-seryl-aspartyl-lysyl-proline in angiotensin II-induced hypertension. Am J Physiol 295:H1253-H1261. doi: 10.1152/ajpheart.00481.2008
77. Liu YH, D'Ambrosio M, Liao TD, Peng H, Rhaleb NE, Sharma U, Andre S, Gabius HJ, Carretero OA (2009) N-Acetyl-seryl-aspartyl-lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am J Physiol 296:H404-H412. doi: 10.1152/ajpheart.00747.2008
78. Peng H, Carretero OA, Peterson EL, Yang XP, Santra K, Rhaleb NE (2012) N-Acetyl-seryl-aspartyl-lysyl-proline inhibits ET-1-induced collagen production by preserving Src homology 2-containing protein tyrosine phosphatase-2 activity in cardiac fibroblasts. Pflugers Arch 464:415-423. doi: 10.1007/s00424-012-1150- 7
79. Rasoul S, Carretero OA, Peng H, Cavasin MA, Zhuo J, Sanchez-Mendoza A, Brigstock DR, Rhaleb NE (2004) Antifibrotic effect of Ac-SDKP and angiotensin-converting enzyme inhibition in hypertension. J Hypertens 22:593-603
80. Rhaleb NE, Pokharel S, Sharma U, Carretero OA (2011) Renal protective effects of N-acetyl-Ser-Asp-Lys-Pro in deoxycorticosterone acetate-salt hypertensive mice. J Hypertens 29:330-338. doi: 10.1097/HJH.0b013e32834103ee
81. Sharma U, Rhaleb N-E, Pokharel S, Harding P, Rasoul S, Peng H, Carretero OA (2008) Novel anti-inflammatory mechanisms of N-Acetyl-Ser-Asp-Lys-Pro in hypertension-induced target organ damage. Am J Physiol 294:H1226-H1232. doi: 10.1152/ajpheart.00305.2007
82. Li P, Xiao HD, Xu J, Ong FS, Kwon M, Roman J, Gal A, Bernstein KE, Fuchs S (2010) Angiotensin-converting enzyme N-terminal inactivation alleviates bleomycin-induced lung injury. Am J Pathol 177:1113-1121. doi: 10.2353/ajpath.2010.081127
83. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG (2007) Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204:2449-2460. doi: 10.1084/jem.20070657
84. Johnson RJ, Herrera-Acosta J, Schreiner GF, Rodriguez-Iturbe B (2002) Subtle acquired renal injury as a mechanism of salt-sensitive hypertension. N Engl J Med 346:913-923. doi: 10.1056/NEJMra011078
85. Ong FS, Lin CX, Campbell DJ, Okwan-Duodu D, Chen X, Blackwell WL, Shah KH, Gonzalez-Villalobos RA, Shen XZ, Fuchs S et al (2012) Increased angiotensin II-induced hypertension and inflammatory cytokines in mice lacking angiotensin-converting enzyme N domain activity. Hypertension 59:283-290. doi: 10.1161/HYPERTENSIONAHA.111.180844
86. Sherman LA, Burke TA, Biggs JA (1992) Extracellular processing of peptide antigens that bind class I major histocompatibility molecules. J Exp Med 175:1221-1226
87. Kozlowski S, Corr M, Takeshita T, Boyd LF, Pendleton CD, Germain RN, Berzofsky JA, Margulies DH (1992) Serum angiotensin-1 converting enzyme activity processes a human immunodeficiency virus 1 gp160 peptide for presentation by major histocompatibility complex class I molecules. J Exp Med 175:1417-1422
88. Nakagawa Y, Takeshita T, Berzofsky JA, Takahashi H (2000) Analysis of the mechanism for extracellular processing in the presentation of human immunodeficiency virus-1 envelope protein-derived peptide to epitope-specific cytotoxic T lymphocytes. Immunology 101:76-82
89. Eisenlohr LC, Bacik I, Bennink JR, Bernstein K, Yewdell JW (1992) Expression of a membrane protease enhances presentation of endogenous antigens to MHC class I-restricted T lymphocytes. Cell 71:963-972
90. Shen XZ, Lukacher AE, Billet S, Williams IR, Bernstein KE (2008) Expression of angiotensin-converting enzyme changes major histocompatibility complex class I peptide presentation by modifying C termini of peptide precursors. J Biol Chem 283:9957-9965. doi: 10.1074/jbc.M709574200
91. Shen XZ, Billet S, Lin C, Okwan-Duodu D, Chen X, Lukacher AE, Bernstein KE (2011) The carboxypeptidase ACE shapes the MHC class I peptide repertoire. Nat Immunol 12:1078-1085. doi: 10.1038/ni.2107
92. Okwan-Duodu D, Datta V, Shen XZ, Goodridge HS, Bernstein EA, Fuchs S, Liu GY, Bernstein KE (2010) Angiotensin-converting enzyme overexpression in mouse myelomonocytic cells augments resistance to Listeria and methicillin-resistant Staphylococcus aureus. J Biol Chem 285:39051-39060. doi: 10.1074/jbc.M110.163782
93. Bennett SM, Broekema NM, Imperiale MJ (2012) BK polyomavirus: emerging pathogen. Microbes and Infection/Institut Pasteur 14:672-683. doi: 10.1016/j.micinf.2012.02.002
94. Kemball CC, Lee ED, Vezys V, Pearson TC, Larsen CP, Lukacher AE (2005) Late priming and variability of epitope-specific CD8+ T cell responses during a persistent virus infection. J Immunol 174:7950-7960
95. Swanson PA 2nd, Lukacher AE, Szomolanyi-Tsuda E (2009) Immunity to polyomavirus infection: the polyomavirus-mouse model. Seminars in Cancer Biology 19:244-251. doi: 10.1016/j.semcancer.2009.02.003
96. Sipahi I, Debanne SM, Rowland DY, Simon DI, Fang JC (2010) Angiotensin-receptor blockade and risk of cancer: meta-analysis of randomised controlled trials. The Lancet Oncology 11:627-636. doi: 10.1016/S1470-2045(10) 70106-6
97. Bangalore S, Kumar S, Kjeldsen SE, Makani H, Grossman E, Wetterslev J, Gupta AK, Sever PS, Gluud C, Messerli FH (2011) Antihypertensive drugs and risk of cancer: network meta-analyses and trial sequential analyses of 324,168 participants from randomised trials. The Lancet Oncology 12:65-82. doi: 10.1016/S1470-2045(10)70260-6
98. Coleman CI, Baker WL, Kluger J, White CM (2008) Antihypertensive medication and their impact on cancer incidence: a mixed treatment comparison meta-analysis of randomized controlled trials. J Hypertens 26:622-629. doi: 10.1097/HJH.0b013e3282f3ef5e
99. Singh A, Bangalore S (2012) Which, if any, antihypertensive agents cause cancer? Curr Opin Cardiol 27:374-380. doi: 10.1097/HCO.0b013e328353bc4f
100. Dive V, Georgiadis D, Matziari M, Makaritis A, Beau F, Cuniasse P, Yiotakis A (2004) Phosphinic peptides as zinc metalloproteinase inhibitors. Cell Mol Life Sci 61:2010-2019. doi: 10.1007/s00018-004-4050-y
101. Redelinghuys P, Nchinda AT, Sturrock ED (2005) Development of domain-selective angiotensin I-converting enzyme inhibitors. Ann N Y Acad Sci 1056:160-175. doi: 10.1196/annals.1352.035